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First published online November 19, 2007
Journal of Experimental Biology 210, 4069-4082 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007096

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Anatomical basis of lingual hydrostatic deformation

Richard J. Gilbert^*, Vitaly J. Napadow, Terry A. Gaige and Van J. Wedeen

Department of Mechanical Engineering, Massachusetts Institute of Technology and the Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Cambridge, MA 02139, USA

View larger version (44K): [in this window] [in a new window]   Fig. 1. Patterns of lingual deformation during swallowing. The swallow is portrayed is a sequence of mid-sagittal images of lingual deformation acquired at 10 Hz using magnetic resonance imaging (MRI, TurboFlash). Shown is a series of images depicting the early accommodation, late accommodation and propulsion phases of the swallow. During early accommodation, an accommodating concavity is created in which the bolus (depicted as a black signal void in the current image sequence) is situated in the anterior oral cavity. With conversion to late accommodation, the concavity is deepened and transferred posteriorly. During the propulsive phase of the swallow, the bolus is propelled retrograde from the oral cavity to the pharynx. Arrow indicates location of the fluid bolus.

View larger version (50K): [in this window] [in a new window]   Fig. 2. Tongue anatomy: classical definitions. (A) Shown here are the intrinsic muscles – that is, the longitudinalis (superior and inferior), transversus and verticalis muscles – in a coronal cross-section of the mammalian tongue. By definition, the intrinsic muscles have no bony attachments, being wholly contained within the tongue. (B) As conventionally defined, the extrinsic muscles insert into the tongue from a superior direction (palatoglossus), postero-superior direction (styloglossus), postero-inferior direction (hyoglossus) and antero-inferior direction (genioglossus). The genioglossus is a large muscle comprising the bulk of the posterior tongue, which originates at the mental spine of the mandible and enters the tongue from below. As noted in the text, while the extrinsic muscles are distinct in their anatomy and physiology at the points of bony attachment, they merge with the intrinsic fibers at the point of insertion into the tongue proper.

View larger version (33K): [in this window] [in a new window]   Fig. 3. Generation of the diffusion tensor. The physical basis for diffusion-weighted imaging is that a magnetic gradient is first dephased and then rephased, and the resulting loss of signal coherence (yielding signal attenuation) represents diffusive motion in the direction of the applied gradient. The set of spatially arrayed diffusion coefficients may be viewed as a second-order tensor, so constituting a method for visualizing 3-D diffusivity in space. The 3-D diffusion tensor may be computed for each voxel and visualized as individual octahedra (A) whose axes are scaled by the size of the eigenvalues and oriented along the corresponding eigenvectors. The principal eigenvector, V1, corresponds to the direction of greatest diffusion, and is equivalent to the principal fiber direction. Octahedra may then be color coded based on the principal eigenvector {x, y, z} mapped to the red–green–blue color space: {|V1x|} (B).

View larger version (67K): [in this window] [in a new window]   Fig. 4. 3-D multislice diffusion tensor MRI representation of the bovine tongue. Coronal slices comprising the bovine tongue obtained by diffusion tensor imaging are shown, with muscle components identified. At each voxel, an octahedron is placed whose shape approximates the local diffusion tensor. The fiber orientation corresponds to the octahedron's long axis and its color to the 3-D orientation. The color code is shown in the color sphere (inset). The sheath consisting of superior and inferior longitudinal muscles is blue, corresponding to its longitudinal fiber orientation, and the tongue core is red and green, corresponding, respectively, to horizontal and vertical fiber orientations, whereas the extrinsic genioglossus and hyoglossus muscles are oblique, and thus coded blue–green. (Reproduced with permission from Wedeen et al., 2001.)

View larger version (125K): [in this window] [in a new window]   Fig. 5. Representation of planar diffusion for the bovine tongue (coronal imaging slice). The orientation of the diffusion tensor's greatest two eigenvectors, the plane of maximum intra-voxel fiber angle dispersion, is represented by the end-planes of graphic cylinders derived from a coronal slice of the lingual core. Contrast was seen between the tongue core, where the planes of fiber angle dispersion were transverse to the antero-posterior axis of the tongue, and the tongue sheath, where these planes were approximately parallel to the nearby tongue surface. (Reproduced with permission from Wedeen et al., 2001.)

View larger version (31K): [in this window] [in a new window]   Fig. 6. Physical basis for diffusion spectrum imaging (DSI). DSI is a high resolution diffusion-weighted imaging technique which determines the complete spin displacement function by acquiring a large number of images with varying diffusion weighting and angularity. This results in the generation of a probability density function (PDF) for the entire set of possible molecular displacements, and thus depicts the set of principal fiber orientations based on the properties of the diffusion maxima. (A) Two sets of model fibers drawn with arbitrary angular separation. (B) In order to simplify the visualization of 3-D diffusion, the PDF is converted to an orientational diffusion function (ODF), which provides a probability distribution for diffusion for a set of angular directions, weighted by the magnitude of the diffusion.

View larger version (71K): [in this window] [in a new window]   Fig. 7. Diffusion spectrum imaging slices obtained from the bovine tongue (axial orientation). Shown are adjacent axial slices of the bovine tongue (A–C, anterior to posterior) obtained by DSI and depicted as a set of 3-D ODFs. Principal fiber directions are color coded (see inset in A), with green indicating the tissue's longitudinal axis, red the vertical axis and blue the transverse axis. (D–F) Selected regions of a single voxel at increased magnification to illustrate ODF detail. (D) Single voxel image showing three distinct crossing fiber populations. (E) Single voxel image showing a single population of fibers, oriented diagonally inward towards the tip of the tongue, exhibiting longitudinal (green) and vertical (red) alignment. (F) Single voxel image showing two crossing fiber populations, orthogonal to each other. (Reproduced with permission from Gilbert et al., 2006.)

View larger version (10K): [in this window] [in a new window]   Fig. 8. Tagged magnetization to assess local tissue deformation. Saturated longitudinal magnetization is applied in two orthogonal directions, which from the sagittal planar perspective (shown here) appears as a rectilinear grid of dark bands amidst the relative brightness of the rest of the MR image. Strain is determined in image post-processing by measuring the amount of deformation undergone by these bands of magnetization during the course of tissue motion.

View larger version (42K): [in this window] [in a new window]   Fig. 9. Visualization of strain derived from tagged magnetization. (A) To obtain local strain from tagged magnetization images, triangular elements are defined by digitizing nodes at tag line intersections. (B) Strain is represented as a pseudosurface whose height denotes the amount of strain for each element of the mesh. (C) The surface is smoothed by the application of a bicubic spline algorithm. (D) The surface is rotated and viewed from above, where the pseudosurface becomes a color-coded strain map.

View larger version (35K): [in this window] [in a new window]   Fig. 10. Tagged magnetization depicting 3-D strain associated with anterior protrusion of the human tongue. (A) A grid of supersaturated MRI tags was applied to the resting tongue in the mid-sagittal imaging plane, and principal strain depicted for the x, y and z components of the strain tensor in terms of a color-coded pseudosurface smoothed by bicubic splines. A bidirectional contraction in the y- and z-directions resulted in tissue protrusion in the x-direction. (B) Model of bidrectional contraction leading to hydrostatic elongation. Contraction of muscle fibers orthogonally aligned to each other results in hydrostatic elongation in the remaining direction (dashed lines), without a change in tissue volume. (Reproduced with permission from Napadow et al., 1999a.)

View larger version (33K): [in this window] [in a new window]   Fig. 11. Mid-sagittal strain imaging during sagittal bending. (A) Employing the approach shown in Fig. 7, the x, y and z normal strain components of the strain tensor are shown. Observe that x-direction and z-direction strain increased and decreased radially from the center of curvature, respectively. (B) Model of hydrostatic lingual tissue bending. The hydrostatic model indicates that tongue bending results from two synergistic mechanisms, unilateral longitudinal sheath contraction and graded intrinsic core fiber contraction which increases with distance from the inside edge. Unilateral sheath contraction results in surface shortening only, without bending, whereas simultaneous sheath and graded core contraction, which maintains x-sectional area by increasing resistance to shear, results in bending. (Reproduced with permission from Napadow et al., 1999a.)

View larger version (103K): [in this window] [in a new window]   Fig. 12. Lingual strain during human swallowing. Direction-dependent strain fields were acquired for the mid-sagittal slice of the tongue during the phases of the swallow, including early accommodation (top row), late accommodation (middle row) and propulsion (bottom row). During early accommodation, bolus containment is associated with negative y-direction strain, consistent with a synergistic contraction of the anterior genioglossus and hyoglossus, with concomitant x- and z-direction expansion. During late accommodation, the combination of y-direction contraction in the posterior tongue and expansion in the anterior tongue results in shifting of the bolus to the posterior dorsal surface of the tongue, consistent principally with contraction of the posterior genioglossus and concomitant x- and z-direction expansion. During propulsion, x- and y-direction expansion in the posterior tongue was consistent with contraction of the laterally inserted styloglossus (with associated passive drag) and z-direction contraction of the posteriorly located transversus fibers. (Reproduced with permission from Napadow et al., 1999b.)

View larger version (28K): [in this window] [in a new window]   Fig. 13. Role of muscular synergy in the generation of lingual deformation. Conceptual drawing depicting the way in which synergistic contractions involving the intrinsic and extrinsic muscles may contribute to prototypical deformations, namely anterior protrusion, bolus accommodation during swallowing and bolus propulsion during swallowing. In each instance, muscle action is viewed from the sagittal, anterior coronal and posterior coronal perspectives. In the case of anterior protrusion, a principal role is played by the simultaneous contractions of the transversus and verticalis muscles, with a secondary role played by the genioglossus (at least in the human). In the case of bolus accommodation during swallowing, a principal role is played by the midline genioglossus fibers, with a secondary role played by the longitudinalis, verticalis and tranversus fibers, which serve to stiffen, broaden and bend the accommodating concavity. In the case of bolus propulsion, a synergistic role is played by the genioglossus, hyoglossus and styloglossus merging with the inferior longitudinalis, as well as the stiffening effect of bidirectional contraction of the core lingual fibers.